THE DISTRIBUTION, HOST PLANTS AND NATURAL ENEMIES OF WHITE PEACH SCALE, PSEUDAULACASPIS
PENTAGONA (TARGIONI-TOZZETTI) (HEMIPTERA:
DIASPIDIDAE), IN ANKARA PROVINCE Ehab Mohammed Ahmed Mahmood Mohammed, Selma Ülgentürk*, Nedim Uygun, A. Pietro Garonna, Ferenc Szenkirály, Meral Fent and Mohammed Hayat * Faculty of Agriculture, Department of Plant Protection, University of Ankara, Ankara, TURKEY. E-mail: ulgentur@ankara.edu.tr
[Mohammed, E. M. A. M., Ülgentürk, S., Uygun, N., Garonna, A. P., Szenkirály, F., Fent, M. & Hayat, M. 2016. The distribution, host plants and natural enemies of white peach scale, Pseudaulacaspis pentagona (Targioni-Tozzetti) (Hemiptera: Diaspididae), in Ankara province. Munis Entomology & Zoology, 11 (2): 650-656]
ABSTRACT: The distribution, host plants, and natural enemies of the white peach scale, Pseudaulacaspis pentagona (Targioni-Tozzetti) (Hemiptera: Diaspididae), were investigated in 25 districts of Ankara Province, Turkey, during 2013-2015. Thirteen districts were infested with harmful white peach scale; infestation was most common in parks, roadsides, private and institution gardens in centrum and old silkroad parts of Ankara. Twenty-two host plant species were found in these 13 districts, five of which (Aesculus carnea, Hibiscus sp., Paulownia tomentosa, Rhus thyphina and Salix babylonica) had not previously been recorded as host plants in Turkey. Some host plant species, including Catalpa bignonioides, Cornus alba, Fraxinus americana, F. excelsior, Forsythia intermedia, Morus alba, M. nigra and Sophora japonica, were found to be very highly infested. Five species of predators and three species of parasitoids were associated with white peach scale. Orius minutus L., Chrysoperla pallida (Henry et al.) are new record as predator of P. pentagona in World and Epitetracnemus comis Noyes &Ren Hui are first time record in Turkey.
KEY WORDS: Rhus thyphina, Salix babylonica, Epitetracnemus comis, Chrysoperla pallida, Orius minutus
The white peach scale (WPS), Pseudaulacaspis pentagona (Targioni-Tozzetti) (Hemiptera: Diaspididae) is covered by a waxy scale that is oval to circular in shape and a creamy-white to reddish-orange in color female. By contrast, adult males are tiny, yellow, two-winged insects. Immature males are also covered with a scale, but this is elongate and snowy white.
WPS is Oriental species and widely distributed all over the world (Garcia et al., 2016). In 1886, this species was seriously pest of mulberry trees and a menace to the silk industry and neighboring countries (Rosen, 1990). After years their spreading towards the north has been observed in central Europe and Mediterranean basin (Bodenheimer, 1953; Kozstarab & Kozár, 1988; Hanks & Denno, 1994; Şişman & Ülgentürk, 2010; Kaydan et al., 2013). It is polyphagous species that infests mulberry, beside of various kinds of deciduous fruit trees, ornamental and wild plants (Ben-Dov et al., 2015). It develops 2-5 generations per year up hanging climatic and geographic conditions (Kosztarab, 1990; Park & Kim, 1990; Branscome, 2012).
WPS is a pest of economic importance for mulberry, peach trees and woody ornamentals. In USA, crop losses from WPS, plus control costs were only $94000, but on the untreated peach trees the yield loss was valued at $480000 (Kosztarab, 1990). In Hawaii, it is only known as a crop pest in papaya (Carica
papaya); WPS poses a serious quarantine problem here, as they move into the
papaya fruit in heavily infested trees (Neumann et al., 2010).
WPS is also attacked by several natural enemies (Collins & Whitcomb, 1975). Some parasites have since provided good control of WPS under most conditions (Collins & Whitcomb, 1975).
WPS is one of the most widely distributed insect species on fruit trees in Turkey (Kozár et al., 1979) and is considered the primary pest for peach trees in the Black Sea region (Kıroğlu, 1981) and the East Mediterranean region (Erkılıç & Uygun, 1997). In Turkey, it has two generations per year in mountainous areas, and three generations per year in coastal areas (Kıroğlu, 1981; Erkılıç & Uygun, 1997). WPS infests fruit plants such as almond, apricot, cherry, kiwi, medlar, mulberry, peach, plum, walnut and ornamental trees in Turkey (Zeki et al., 2004; Ülgentürk et al., 2009; Kaydan et al., 2013).
In recent years, WPS has also become a pest of great importance for mulberry trees (Morus spp.) in Ankara, due to the increased number of mulberry. This study aims to find out the size and spread of this insect and also determine the possibility of using biological control elements within integrated control program in Ankara province.
MATERIALS AND METHODS
Surveys were conducted to determine the distribution, host plants, and natural enemies of WPS in 17 districts and eight areas of Centrum of Ankara in the Spring–Autumn period of 2013-2015 (Fig. 1). Sampling areas were randomly selected, and infested twigs and/or branches were collected and placed in labelled plastic bags. The samples were then taken to the laboratory and examined under a stereomicroscope. Some WPS females were placed in 70% ethyl alcohol for identification, while others were put into plastic jars to rear their natural enemies. Adult predators of WPS that were found feeding with WPS on the same plant were collected directly by hand, while immature stages were reared on the WPS in climate room. The identification of host plants was made by the Landscape Department of Faculty of Agriculture, University of Ankara, Turkey.
RESULTS AND DISCUSSION
In total, 23 host plant species of WPS were found in 13 districts of Ankara province in 2013-2015. 7 of them were fruit trees (Juglans regia, Morus alba, M.
nigra, Prunus avium, P. persica, Vitis vinifera, Ficus carica), while 16 were
woody ornamental trees (Aesculus carnea, Catalpa bignonioides, Cornus alba,
Forsythia intermedia, Fraxinus americana, F. excelsior, Hibiscus syriacus, Koelreuteria paniculata, Paulownia tomentosa, Rhus thyphina var. laciniata, Ribes aureum, Robinia pseudoacacia, Salix babylonica, Sophora japonica, Syringa vulgaris, and Tilia tomentosa) and one ornamental species Pelargonium peltatum (Table 1). WPS was determined to very high level infestation in centrum
of Ankara and some districts, especially Ayaş, Beypazarı, Nallıhan on old silkroad with C. bignonioides, Cornus spp., Forsythia intermedia, Fraxinus spp., M. alba,
M. nigra, and S. japonica, being most common. While P. peltatum, R. thyphina
var. laciniata, S. babylonica, Ficus carica and V. vinifera were found rare host plant with high infestation. Interestingly, Fraxinus americana, F. excelsior,
Hibiscus sp., P. peltatum, V. vinifera, Paulownia tomentosa, A. carnea, R. thyphina var. laciniata and S. babylonica are found for the first time as host
plants of WSP in Ankara and last four of them are recorded for the first time in Turkey.
In Ankara, Crataegus oxyacantha, C. bignonioides, F. intermedia, K.
paniculata, M. alba, M. nigra var. pendula, R. aureum, S. japonica, S. vulgaris
have been recorded by previous researchers as host of WSP (Çobanoğlu & Düzgüneş 1986; Ülgentürk & Toros, 1996; Ülgentürk & Toros, 2000; Zeki et al., 2004). In Aegean, Black Sea, Central Anatolia, Marmara and Mediterranean regions of Turkey, many fruit and ornamental plant species like Actinia chinensis,
A. deliciosa, Aesculus sp., Ailanthus altissima, Buxus sempervirens, Prunus avium, P. amygdalus, P. laurocerasus, Pelarganium sp., Ribes aureum, Robinia pseudoacacia, Tamarix sp., Sophora japonica, Syringia, vulgaris and V. vinifera were found as host plants of WPS (Çanakçıoğlu, 1977; Kıroğlu, 1981;
Erkılıç & Uygun, 1995; Ülgentürk & Çanakçıoğlu, 2004; Ülgentürk et al., 2009). P.
pentagona is a cosmopolitan and polyphagous scale insect, and its wide range
host spectrum points its adaptation and survival capacity.
In these study 5 species are found as predators of WPS; Orius minutus L.
(Hemiptera: Anthocoridae), Chilocorus bipustulatus L., Brumus
quadripustulatus L. (Coleoptera: Coccinellidae), Cybocephalus sp. (Coleoptera:
Cybocephalidae) and Chrysoperla pallida (Henry et al.) (Neuroptera: Chrysopidae). The most common predator is C. bipustulatus followed by
Cybocephalus sp. whereas the other predators are in few numbers. C. bipustulatus and Cybocephalus sp. are well known general predators on WPS and
other scale insects in Turkey and all the world (Soylu & Ürel, 1977; Kıroğlu, 1981; Koztarab & Kozar 1988; Erkılıç & Uygun, 1995; Erler & Tunç, 2001; Ülgentürk & Toros, 2001). In spring, C. bipustulatus had controlled successfully of population of WSP but this success was not permanently in peach orchards of Black Sea region (Kıroğlu, 1981). The other general predators are Chrysoperla pallidus and
Orius minutus are detected first time on WPS in Turkey and the world. Both
predators prey mites, thrips, whiteflies, aphids, many other soft-bodied arthropods and their immature stages (Soylu & Ürel, 1977; Hagen et al., 1999; Efe et al., 2015). Graora & Spasić (2008) were recorded first time Chrysopa carnea Stephens and Deraeocoris ruber Linnaeus feeding P. pentagona. We think omnivorous characters of these predators are limited to control of WPS populations in Ankara.
As parasitoid of white peach scale, 3 species namely Aphytis proclia (Walker),
Encarsia berlesei (Howard) (Hymenoptera: Aphelinidae) and Epitetracnemus comis Noyes & Ren Hui (Hymenoptera: Encyrtidae) were found in Ankara. E. berlesei and A. proclia are common respectively while E. comis is few number in
Ankara. This parasitoid is recorded for the first time in Turkey. E. berlesei is thelytokous, endophagous parasitoids, reproducing young female and both immature stages of WPS (Bennassy, 1958; Habibian & Assadi, 1989; Pedata et al., 1995). E. berlesei was introduced to Italy from Japan and U.S.A. for the control of heavy infestation of WPS on mulberry trees that use silk production. Releasing of
E. berlesei was complete success in Italy and parasitoid distributed all over the
areas in Europe (Rosen, 1990). E. berlesei was the most abundant parasitoid of WPS in Italian orchards (Goranna & Viggiani, 1997). According Bodenheimer (1958), few number of E. berlesei from Florida was introduced to control WSP on mulberry trees that used silk production in Bursa by director of Silk research Institute in in year 1930. Releasing was limited success in the beginning. Although E. berlesi was most common parasitoid of WPS in Antalya (Erler & Tunç, 2001), surprisingly it was unsufficient to control WPS on peach in Black sea region (Kıroğlu, 1981) and in Mediteranean, Turkey (Erkılıç & Uygun, 1995).
Gürkan (1982) reported E. (Praspaltella) berlesei and Aphytis diaspidis Howard were parasited 57.4% of P. pentagona of population in Marmara region.
General ectoparasitoid, A. proclia was recorded in the previous work in Ankara (Ülgentürk & Toros, 2001). Benassy (1961) was conducted ectoparasitoids like Aphytis were highly dependent on climatic influences. Endoparasitod species like Encarsia more dependent their host than climatic conditions. Graora & Spasić (2008) were reported E. berlesei and A. proclia were found to be the most important regulators of P. pentagona population density with parasitism mounting to 60, even 64% in Serbia.
As a result of this study, among the 25 areas in Ankara, only 13 of them were infected with P. pentagona, 22 plant species has been found infected with armored insect. 4 of them are recorded for the first time in Turkey. In the affected areas with P. pentagona, 5 predators and 3 parasites were recorded. 2 predators and 1 parasite were not recorded in Turkey before. In a future study there is hope to see the relationship between E. berlesei and the WPS, and the extent of its ability to control this pest.
ACKNOWLEDGEMENTS
The authors are grateful Dr. M. Spodek, The Steinhardt Museum of Natural History Israel National Center for Biodiversity Studies , for kindly reading the manuscript and for his valuable suggestions.
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Table 1. Host plants of white peach scale (Pseudaulacaspis pentagona) in Ankara Province.
District Host plant Location / date
Altındağ Cornus alba, C. alba, Fraxinus americana
Forsythia intermedia, Juglans regia, Morus alba, M. nigra, Prunus avium, Sophora japonica, Syringa vulgaris
Altın Park, 25.08.2013
M. nigra var. pendula Gençlik Park, 16.08.2014 M. alba var. pendula, Paulownia
tomentosa Ankara Railway Station Garden, 16.08.2014
M.nigra Hasköy, 03.06.2015
S. japonica Aydınlık Evler, 03.06.2015
Ayaş M. alba Centrum, 12.04.2013
Beypazarı Ficus carica, M. alba, Salix babylonica,
S. japonica Centrum, 21.09.2015
Cayırhan Paulownia tomentosa, M. alba Cumhuriyet Park, 21.9.2015 Çankaya Aesculus x carnea, Catalpa bignonioides,
C. alba, F. excelsior, F. intermedia, J. regia, Koelreuteria paniculata, M. alba, M. nigra, Robinia pseudoacacia, S. japonica, Tilia tometosa
Dikmen Park 1, 2 Etap, 27.09.2013
M. alba Birlik quarter, 28.09.2014
M. alba Oran quarter, 28.10.2014
F. americana, S. japonica, Koelreuteria
paniculata, M. nigra, Prunus persica Kurtuluş Park, 25.09.2013 M. alba, P. tomentosa Tandoğan, 01.10.2013
M. alba Ahlâtlıbel, 28.09.2015
M. alba Ulus Kale, 03.08.2014
M. alba, M. nigra Botanik Park, 20.04.2013
M. nigra Seğmenler Park, 20.04.2015
S. japonica İncek, 20.4.2015
M. alba, M. nigra Hoşdere, 20.04.2015
Çubuk S. japonica Esenboğa Airport Road ,
30.06.2015
Gölbaşı M. alba Centrum
Hacıhasan village, 17.04.2013 M. alba
F. excelsior Eymir Forest, 13.03.2014
Keçiören J. regia , M. alba, M. nigra İncirli Basınevler Park, 12.06.2013
C. bignonioides, C. alba, F. excelsior, F. intermedia, Hibiscus syriacus, M. alba, M. nigra
Faculty of Agriculture /Campus, 23.05.2015
Fraxinus excelsior Ankara University Campus General Directorate of Meteorology /garden Keçiören Casino Park, 18.05.2015
M. alba S. japonica
S. japonica Sanatoryum Hastanesi Bahçesi,
06.06.2015 Mamak F. intermedia, M. nigra , S. japonica, S.
vulgaris Ankara Üniversitesi Dikimevi- Campus, 25.09.2013 R. pseudoacacia Samsun Highway, 15.09.2014 Nallıhan C. bignonioides, F. intermedia, M.
nigra, M. alba, Prunus persica, Vitis vinifera
Centrum and road, 21.09.2015 Polatlı M. alba, R. pseudoacacia, S. japonica Centrum, 20.09.2014
Pursaklar C. bignonioides, M. alba Bağla quarter, 15.05.2013 Yenimahalle M. alba, S. japonica, S. vulgaris TAGEM / garden, 10.07.2013
C. bignonioides, C. alba, F. intermedia, F. americana, M. alba, M. nigra, J. regia
Demetevler Cemre Park, 12.06.2013
C. bignonioides, Ribes aureum Ministry of Agriculture Logistics Facilities/ garden, 15.11.2013 Table 2. Predators of white peach scale (Pseudaulacaspis pentagona) in Ankara Province.
Predator Date / location Host plant
Chilocorus bipustulatus L. Morus alba, 26.08.2014, Altınpark; M. alba var. pendula, M. alba, Morus alba, 12.04.2013, Oran Aesculus hippocastanum, Catalpa bignonioides, Cornus alba, Fraxinus americana, M. alba, M. alba var. pendula, Morus nigra, Robinia pseudoacacia, S. japonica, 27.09.2015, Dikmen 1, 2 etap; C. bignonioides, Fraxinus excelsior, M. alba, Morus nigra var. pendula, 23.05.2015, Ankara University Campus, Tandoğan; M. alba, C. bignonioides, 17.05.2015, Faculty of Agriculture Campus; S. japonica 25.09.2014, Ankara University Dikimevi Campus; C. bignonioides, F. americana, M. alba, 10.08.2014, Cemre park; C. bignonioides, 15.11.2015, Campus of Agriculture, Yenimahalle Brumus quadripustulatus L. M. alba, 15.11.2015, Campus of Agriculture, Yenimahalle Cybocephlus sp. M. alba, 26.08.2014, Altınpark; Morus alba, 12.04.2013,
Oran; M. alba, 12.07.2014, Seymenler park; M. alba, S. japonica, 23.05.2015, Ankara University Campus, Tandoğan; Forsythia intermedia, F. excelsior, 17.05.2015, Faculty of Agriculture Campus; C. bignonioides, M. alba, 21.09.2015, Centrum: M. alba, Cemrepark Demetevler, Ankara, 21.10.2015
Orius minutus L. F. excelsa, 20.07.2015; F. excels, 22.09.2015; Altınpark, M. alba, Salix babylonica, 21.09.2015, Beypazarı Chrysoperla pallida (Henry et
al.) M. alba, 21.09.2015, Botanik park
Table 3. Parazitoits of white peach scale (Pseudaulacaspis pentagona) in Ankara province. Parazitoit Location / Date Host plant
Aphytis proclia (Walker) M. alba, Ayaş, 24.03.2013; M. alba, Ayaş, 13.05.2013; M. alba, Bağlar, 11.06.2013; M. alba, Cemrepark Demetevler, Ankara, 21.10.2015
Encarsia berlesei (Howard) M. alba, Altınpark, 22.05.2013; M. alba, Bağlar, 20.05.2013; M. alba, Ayaş, 13.05.2013; M. alba, Botanik park, 10.05.2013; M. alba, Gölbaşı, 03.04.2013 Epitetracnemus comis Noyes&